Abstract
Insect mate recognition is often viewed as stereotypic, innate, and species-specific. However, male damselflies can learn to identify female-specific color morphs as potential mates. A suite of male mimicry hypotheses assume that heteromorphic females, which differ from males in color pattern, are more easily recognized as “female” and thus lack the inherent, anti-harassment advantage that the more male-like signal provides for andromorphs. Using two measures of male preference, we investigated whether naïve males have a preexisting sensory bias for a given morph color in Enallagma civile, a species that appeared to exhibit extreme plasticity in morph expression across generations within a breeding season. E. civile males raised in the absence of females exhibited no preference for either morph, whereas males raised with one female type exhibited a learned sensory bias for that morph. Male Enallagma also lacked a bias toward conspecific females over a congeneric sister species. In a naturally naïve population of Enallagma ebrium, males reacted sexually to both morphs of Enallagma hageni as often as they did to conspecific females, whose thoracic spectra were nearly identical with those of E. hageni. Moreover, despite the similar thoracic spectra of males and andromorphs, both of which reflected UV, males rarely reacted sexually to other males. Our results falsified implicit assumptions of male mimicry hypotheses, supported learned mate recognition, and suggested a scenario for speciation via sexual conflict.
Similar content being viewed by others
References
Andrés JA, Cordero A (1999) The inheritance of female colour morphs in the damselfly Ceriagrion tenellum (Odonata, Coengrionidae). Heredity 82:328–335
Arnqvist G, Rowe L (1995) Sexual conflict and arms races between the sexes: a morphological adaptation for control of mating in a female insect. Proc R Soc Lond Ser B 261:123–127
Arnqvist G, Edvardsson M, Friberg U, Nilsson T (2000) Sexual conflict promotes speciation in insects. Proc Natl Acad Sci USA 97:10460–10464
Beukema JJ (2004) Recognition of conspecific females by males of Calopteryx haemorrhoidalis (Vander Linden)(Zygoptera: Calopterygidae). Odonatologica 33:147–156
Bick GH, Bick JC (1963) Behavior and population structure of the damselfly, Enallagma civile (Hagen) (Odonata Coenagrionidae). Southwest Nat 8:57–84
Bick GH, Hornuff LE (1966) Reproductive behavior in the damselflies Enallagma aspersum (Hagen) and Enallagma exsulans (Hagen) (Odonata: Coenagrionidae). Proc Entomol Soc Wash 68:78–85
Bond AB, Kamil AC (2002) Visual predators select for crypticity and polymorphism in virtual prey. Nature 415:609–613
Chapman RF (1971) The Insects: structure and function. Elsevier, New York
Charlton RE, Webster FX, Zhang A, Schal C, Liang D, Sreng I, Roelofs WL (1993) Sex pheromone of the brownbanded cockroach is an unusual dialkyl-substituted alpha-pyrone. Proc Natl Acad Sci USA 90:10202–10205
Corbet PS (1999) Dragonflies: behavior and ecology of Odonata. Cornell University Press, Ithaca, NY
Cordero A (1989) Reproductive behaviour of Ischnura graellsii (Rambur) (Zygoptera: Coenagrionidae). Odonatologica 18:237–244
Cordero A (1990) The inheritance of female polymorphism in the damselfly Ischnura graellsii (Rambur) (Odonata: Coenagrionidae). Heredity 64:341–346
Cunningham JP, West SA, Zalucki (2001) Host selection in phytophagous insects: a new explanation for learning in adults. Oikos 95:537–543
Dukas R (2005) Experience improves courtship in male fruit flies. Anim Behav 69:1203–1209
Dukas R, Bernays EA (2000) Learning improves growth rate in grasshopper. Proc NatL Acad Sci USA 97:2637–2640
Dunkle SW (1990) Damselflies of Florida, Bermuda and the Bahamas. Scientific, Gainesville
Endler JA (1993) On the measurement and classification of colour in studies of animal colour patterns. Biol J Linn Soc 41:315–352
Fincke OM (1982) Lifetime mating success in a natural population of the damselfly, Enallagma hageni (Walsh) (Odonata: Coenagrionidae). Behav Ecol Sociobiol 10:293–302
Fincke OM (1986) Lifetime reproductive success and the opportunity for selection in a nonterritorial damselfly (Odonata: Coenagrionidae). Evolution 40:791–803
Fincke OM (1994) Female dimorphism in damselflies: failure to reject the null hypothesis. Anim Behav 47:1249–1266
Fincke OM (1997) Conflict resolution in the Odonata: implications for understanding female mating patterns and female choice. Biol J Linn Soc 60:201–220
Fincke OM (2004) Polymorphic signals of harassed female odonates and the males that learn them support a novel frequency-dependent model. Anim Behav 67:833–845
Fincke OM, Jödicke R, Paulson DR, Schultz TD (2005) The evolution and frequency of female color morphs in Holarctic Odonata: why are male-like females typically the minority? Inter J Odonatol 8:183–212
Fric Z, Konvicka M, Zrzavy J (2004) Red & black or black & white? Phylogeny of Araschnia butterflies (Lepidoptera: Nymphalidae) and evolution of seasonal polymorphism. J Evol Biol 17:265–278
Gavrilets S, Waxman D (2002) Sympatric speciation by sexual conflict. Proc Natl Acad Sci USA 99:10533–10538
Gavrilets S, Arnqvist G, Friberg U (2001) The evolution of female mate choice by sexual conflict. Proc R Soc Lond B 268:531–539
Gemeno C, Schal C (2004) Sex pheromones of cockroaches. In: Cardè RT Millar JG (eds) Advances in insect chemical ecology. Cambridge University Press, New York pp 179–247
Godfray HCJ, Waage JK (1988) Learning in parasitic wasps. Nature 331:211
Gorb SN (1998) Visual cues in mate recognition by males of the damselfly Coenagrion puella (L.) (Odonata: Coengarionidae). J Insect Behav 11:73–92
Greenfield MD (2002) Signalers and receivers: mechanisms and evolution of arthropod communication. Oxford University Press, Oxford, UK
Hebets EA (2003) Subadult experience influences adult mate choice in an arthropod: exposed female wolf spiders prefer males of a familiar phenotype. Proc Natl Acad Sci USA 100:13390–13395
Hinnekint BON (1987) Population dynamics of Ischnura e. elegans (Vander Linden) (Insecta: Odonata) with special reference to morphological colour changes, female polymorphism, multiannual cycles and their influence on behaviour. Hydrobiology 146:3–31
Holland B, Rice WR (1999) Experimental removal of sexual selection reversed intersexual antagonistic coevolution and removes a reproductive load. Proc Natl Acad Sci USA 96:5083–5088
Irwin DE, Price T (1999) Sexual imprinting, learning, and speciation. Heredity 82:347–354
Jacobson M (1972) Insect sex pheromones. Academic, New York
Johnson C (1964) The inheritance of the female dimorphism in the damselfly, Ischnura damula. Genetics 49:513–519
Johnson C (1966) Genetics of female dimorphism in Ischnura demorsa. Heredity 21:453–459
Johnson C (1975) Polymorphism and natural selection in ischnuran damselflies. Evol Theory 1:81–90
Labhart T, Nilsson D-E (1995) The dorsal eye of the dragonflies Sympetrum: specializations for prey detection against the blue sky. J Comp Physiol A 176:437–453
Lam E (2004) Damselflies of the northeast: a guide to the species of eastern Canada and the northeastern United States. Biodiversity Books, Forest Hills, NY
Magurran AE, Ramnarine IW (2004) Learned mate recognition and reproductive isolation in guppies. Anim Behav 67:1077–1082
McLain KD, Pratt AE (1999) The cost of sexual coercion and heterospecific sexual harassment on the fecundity of host-specific, seed-eating insect (Neacoryphyus bicrucis) Behav Ecol Sociobiol 46:164–170
Miller MN, Fincke OM (1999) Cues for mate recognition and the effect of prior experience on mate recognition in Enallagma damselflies. J Insect Behav 12:801–814
Miller MN, Fincke OM (2004) Mistakes in sexual recognition among sympatric zygoptera vary with time of day and color morphism (Odonata: Coenagrionidae). Intl J Odonatol 7:471–491
Nielsen MG, Watt WB (2000) Interference competition and sexual selection promote polymorphism in Colias (Lepidoptera, Pieridae). Funct Ecol 14:718–730
Oxford GS, Gillespie RG (1998) Color polymorphisms in spiders. Annu Rev Entomol 43:619–643
Panhuis TM, Butlin R, Zuk M, Tregenza T (2001) Sexual selection and speciation. Trends Ecol Evol 16:364–371
Paulson DR (1974) Reproductive isolation in damselflies. Syst Zool 23:40–49
Papaj DR, Prokopy RJ (1989) Ecological and evolutionary aspects of learning in phytophagous insects. Annu Rev Entomol 34:315–350
Phelan PL (1997) Evolution of mate-signaling in moths: phylogenetic considerations and predictions from the asymmetric tracking hypothesis. In: Choe CJ, Crespi BJ (eds) The evolution of mating systems in insects and arachnids. Cambridge University Press, Cambridge, UK, pp 240–256
Robertson HM (1985) Female dimorphisms and mating behaviour in a damselfly, Ischnura ramburii: females mimicking males. Anim Behav 33:805–809
Robertson HM, Paterson HEH (1982) Mate recognition and mechanical isolation in Enallagma damselflies (Odonata: Coenagrionidae). Evolution 36:243–250
Ryan MJ (1998) Sexual selection, receiver biases, and the evolution of sex differences. Science 281:1999–2003
Sánchez-Guillén RA, Van Gossum H, Cordero Rivera A (2005) Hybridization and the inheritance of female colour polymorphism in two ischnurid damselflies (Odonata: Coenagrionidae). Biol J Linn Soc 85:471–481
Sirot LK, Brockman HJ (2001) Costs of sexual interactions to females in Rambur’s forktail damselfly, Ischnura ramburi (Zygoptera: Coenagrionidae). Anim Behav 61:415–424
Sirot LK, Brockmann HJ, Marinis C, Muschett G (2003) Maintenance of a female-limited polymorphism in Ischnura ramburi (Zygoptera: Coenagrionidae). Anim Behav 66:763–775
Sherratt TN (2001) The evolution of female-limited polymorphisms in damselflies: a signal detection model. Ecol Lett 4:22–29
Slagsvold T, Hansen BT, Johannessen LE, Lifjeld JT (2002) Mate choice and imprinting in birds studied by cross-fostering in the wild. Proc R Soc Lond B 269:1449–1455
Svensson EI, Abbott J, Härdling R (2005) Female polymorphism, frequency dependence, and rapid evolutionary dynamics in natural populations. Am Nat 165:567–576
Turgeon J, McPeek M (2002) Phylogenetic analysis of a recent radiation of Enallagma damselflies (Odonata: Coenagrionidae). Mol Ecol 11:1989–2001
Turgeon JR, Soks RA, Thum JM, Brown, McPeek MA (2005) Simultaneous quaternary radiations of three damselfly clades across the Holarctic. Am Nat 165:78–107
Van Gossum H, Stoks R, Matthysen E, Valck F, De Bruyn L (1999) Male choice for female colour morphs in Ischnura elegans (Odonata: Coenagrionidae): testing the hypotheses. Anim Behav 57:1229–1232
Van Gossum H, Stoks R, De Bruyn L (2001a) Reversible frequency-dependent switches in male mate choice. Proc R Soc Lond B 268:83–85
Van Gossum H, Stoks R, De Bruyn L (2001b) Frequency dependent male mate harassment and intra-specific variation in its avoidance by females of the damselfly, Ischnura elegans. Behav Ecol Sociobiol 51:69–75
Van Gossum H, DeBruyn L, Stoks R (2005a) Reversible switches between male–male and male–female mating behaviour by male damselflies. Biol Lett 1:268–270
Van Gossum H, DeBruyn L, Stoks R (2005b) Male harassment on female colour morphs in Ischnura elegans (Vander Linden): testing two frequency-dependent hypotheses (Zygoptera: Coenagrionidae). Odonatologica 34:407–414
Walker EM (1953) The Odonata of Canada and Alaska, Vol. I. University of Toronto, Toronto
Watson P, Arnqvist G, Stallmann RR (1998) Sexual conflict and the energetic costs of mating and mate choice in water striders. Am Nat 151:46–58
Weiss MR, Papaj DR (2003) Colour learning in two behavioural contexts: how much can a butterfly keep in mind? Anim Behav 65:425–434
Wiklund C, Tullberg BS (2004) Seasonal polyphenism and leaf mimicry in the common butterfly. Anim Behav 68:621–627
Yang EC, Osorio D (1996) Spectral responses and chromatic processing in the dragonfly lamina. J Comp Physiol A 178:5443–550
Acknowledgements
We thank J. Chou, C. Jalicon, C. Marsh, B. Mollard, R. Smith, and R. Zamor for field assistance; the University of Oklahoma for financial support; and three anonymous reviewers for constructive comments.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by P. Moore
Rights and permissions
About this article
Cite this article
Fincke, O.M., Fargevieille, A. & Schultz, T.D. Lack of innate preference for morph and species identity in mate-searching Enallagma damselflies. Behav Ecol Sociobiol 61, 1121–1131 (2007). https://doi.org/10.1007/s00265-006-0345-3
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00265-006-0345-3